Uktena riparia, Fend, Rodriguez & Lenat, 2015

Rodriguez, Pilar & Fend, Steven V., 2018, On spermatophore-producing aquatic microdrile oligochaetes (Annelida: Clitellata), Zootaxa 4497 (1), pp. 41-60 : 51-52

Uktena riparia

( Figure 5 )

In this lumbriculid species, both well-developed spermathecae (filled with sperm) and spermatophores are present. Spermathophores in U. riparia are long, thin tubes ( Fig. 5A,B ); they develop in the atrial duct ( Fig. 5F ), apparently using secretions from a section of the atrial ampulla that has a specialized, highly folded epithelium and unsually elongate prostatic glands ( Fig. 5E ; Fend et al. 2015: Fig. 4J–L ). Therefore, the spermatophores appear wholly formed within the male bursa, before being transferred to the spermathecal bursa of the partner. As in other microdrile species producing spermatophores, several glandular organs are associated with both male and spermathecal bursae ( Fig. 5C,D ). A muscular copulatory organ within the spermathecal bursa (protruded in Fig. 5A ) is probably related to the transfer and attachment of the spermatophores to the concopulant, using a secretion from a large basal gland ( Fig. 5C ; Fend et al. 2015: Fig. 3H,L,M ). When transferred, spermatophores are attached at the base of the partner's copulatory organ, and positioned inside the spermathecal bursa with one end close to the entrance to the spermathecal duct ( Fig. 5C ). Then, the sperm leave the spermatophore and directly pass to the spermatheca ( Fend et al. 2015: Figs. 2A–C , 3 I,L ).

Sperm transfer by spermatophores is otherwise unknown in microdrile oligochaetes with well-developed spermathecae, although it has been described in some megadriles ( Omodeo & Rota 1989). The use of spermatophores to transfer sperm from the male duct to the spermatheca, instead of a more typical mating behavior involving a direct sperm transfer by opposition of male and spermathecal pores, suggests an unusual mating behavior and a specific function of the spermatophores (see discussion).

The rare occurrence of sperm transfer through spermatophores in microdriles contrasts with its common occurrence in rhynchobdellid leeches. Evolutionary derivation of leeches from a lumbriculid-like ancestor had been suggested by several phylogenetic studies based on morphological characters (Brinkhurst & Nemec 1987; Jamieson et al. 1987) and most recently, by molecular analyses ( Erséus 2005; Martin 2000; Siddall et al. 2001). The formation of spermatophores in the lining atrial epithelium of the lumbriculid U. riparia suggests an additional approach to investigating the relationships of leeches and lumbriculids.

Figures

FIGURE 2. Bothrioneurum species. A–E. B. vejdovskyanum Štolc, 1886 (from Tarmo Timm's collection). A. Spermatophore attached to the clitellar region. B. Atrium with a diffuse layer of prostatic cells. C,D. Copulatory organ (= paratrium). E. Developing sperm morulae in the coelom (composed from 2 photos). F–J. B. brauni Marcus, 1949 (Marchese's collection). F. Spermatophore capsule. G. Detail of sperm funnel and atrium. H. Junction of atrium and ental section of the copulatory bursa. I,J. Copulatory organ (= paratrium) with conical projection of glands to the copulatory bursa. B, D, G–J histological sections. Abbreviations: a atrium, cb copulatory bursa, gl gland, m muscular layer, pa paratrium, pr prostatic cells, sf sperm funnel, t testis, vd vas deferens.

FIGURE 3. Paranadrilus descolei Gavrilov, 1955. A–G,I,J from Marchese's collection, H,K,L from Gavrilov's collection. A. Anterior part of the body. B. Ventral gland in the posterior part of segment V. C. Spermatophores within a lateral pouch in the anterior part of segment XII. D. Detail of the attachment of the spermatophores within the pouch. E. Transverse section of the empty spermatophore pouch. F. Sperm funnel and male pore slit. G. Bulbous male sac containing the copulatory organ, and empty spermatophore pouch behind septum 11/12. H. Scarcely developed male sac containing a long copulatory organ covered by a chitinous layer in a dissected specimen from Gavrilov's type collection. I. Male sac with copulatory organ and copulatory bursa. J. Spermatophore in the ental part of the copulatory bursa. K,L. Segment XI of the lectotype of P. descolei, showing the large ovary, the bulbous male sac filled by glandular secretions and spermatozoids, and the copulatory bursa with folded walls. A,E,G,I–L, histological sections. Abbreviations: at attachment site, cb copulatory bursa, co copulatory organ, ed ejaculatory duct, m muscular layer, mp male pore, ms male sac, o ovary, ph pharynx, sf sperm funnel, sp spermatophore pouch, sph spermatophore, vd vas deferens.

FIGURE 4. Aktedrilus species forming spermatophores (from Swedish Museum of Natural History collection). A. A. mediterraneus (Erséus, 1980), spermatophore in segment XI. B–C. A. arcticus (Erséus, 1978), histological sections of the male duct. D. A. labeosus (Baker & Erséus, 1982), copulatory bursa and glandular organ. E,F. A. mediterraneus, histological sections of the male duct. Abbreviations: a atrium, cb copulatory bursa, go glandular organ, gr glandular ring, ms male sac, o ovary, sf sperm funnel, sph spermatophore, vd vas deferens.

FIGURE 5. Uktena riparia Fend, Rodriguez & Lenat, 2015. A. Ventral side showing 2 stained spermatophores attached to the base of a protruded copulatory organ. B. Detail of the spermatophore protruding from male pore, and genital chaetae. C. Copulatory organ and associated gland within the spermathecal bursa, with spermatophores attached to its base. D. Male bursa with showing one of the several glandular organs. E. Detail of the atrium showing folded epithelium and long prostatic glands. F. Spermatophore forming in the atrial duct. G. Sperm lined up along the epithelium of the spermathecal ampulla. A,C,E from Fend's coll.; D,F,G from MNCN collection; all from the type locality. Abbreviations: a atrium, co copulatory organ, gc genital chaetae, gl gland, mb male bursa, mp male pore, pr prostatic cells, sb spermathecal bursa, sph spermatophore, ssg secretory surface of the gland.